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Just do it! How performing an action enhances remembering in transient global amnesia.
Mathieu Hainselin, Peggy Quinette, Aurelija Juskenaite, Béatrice Desgranges, Olivier Martinaud, Vincent de la Sayette, Didier Hannequin, Fausto Viader,
Francis Eustache
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Mathieu Hainselin, Peggy Quinette, Aurelija Juskenaite, Béatrice Desgranges, Olivier Martinaud, et
al.. Just do it! How performing an action enhances remembering in transient global amnesia.. Cortex,
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Note
Just do it! How performing an action enhances remembering in transient global amnesia
Mathieu Hainselin
a,b,c,d, Peggy Quinette
a,b,c,d, Aurelija Juskenaite
a,b,c,d, Be´atrice Desgranges
a,b,c,d, Olivier Martinaud
f, Vincent de La Sayette
a,b,c,e, Didier Hannequin
f,g, Fausto Viader
a,b,c,eand Francis Eustache
a,b,c,d,*
aInserm, U1077, Caen, France
bUniversite´ de Caen Basse-Normandie, UMR-S1077, Caen, France
cEcole Pratique des Hautes Etudes, UMR-S1077, Caen, France
dCHU de Caen, U1077, Caen, France
eCHU de Caen, Service de Neurologie, Caen, France
fCHU de Rouen, Rouen, France
gInserm, U1079, Rouen, France
a r t i c l e i n f o
Article history:
Received 5 March 2013 Reviewed 5 May 2013 Revised 2 August 2013 Accepted 21 October 2013 Action editor Georg Goldenberg Published online 30 October 2013
Keywords:
Transient global amnesia Enactment effect Self-performed task Binding
Memory for action
a b s t r a c t
Transient global amnesia (TGA) is a clinical syndrome characterized by the sudden onset of a massive episodic memory deficit that spares other cognitive functions. As such, it provides a unique human amnesia model for testing the enactment effect (i.e., better memory for performed actions than for verbally encoded sentences). Our main aim was to test whether the enactment effect is preserved in TGA patients, both to have a better understanding and to test the robustness of this effect in a massive amnesia.
Object-action pairs were encoded under four conditions: verbal, experimenter- performed, and two enacted conditions (self-performed and self-performed with choice).
We tested object-action pair retrieval using cued recall (CR) and recognition tasks, and source memory using a free recall task. We also assessed binding, executive functions, short-term memory, episodic memory, anxiety and mood. We run correlations to control for their putative effects on memory for action. Data were collected from 24 patients, 16 of whom were examined during the acute phase and eight the day-after, as well as from 18 healthy controls.
The memory performances of the patients in the acute phase improved for both i) the CR score, between the verbal, experimenter-performed and self-performed with choice conditions, and ii) the total recognition score, between the verbal condition and the two enacted conditions. Correlations were found between self-performed task (SPT) enhance- ment and both the binding and anxiety.
*Corresponding author. InsermeEPHEeUniversite´ de Caen Basse-Normandie, Unite´ de recherche U1077, “Neuropsychologie et neu- roanatomie fonctionnelle de la me´moire humaine”, CHU, Avenue de la Coˆte de Nacre, 14033 Caen Cedex 09, France.
E-mail addresses:neuropsycho@chu-caen.fr,francis.eustache@inserm.fr(F. Eustache).
Available online at www.sciencedirect.com
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Journal homepage:www.elsevier.com/locate/cortex c o r t e x 5 0 ( 2 0 1 4 ) 1 9 2e1 9 9
0010-9452/$esee front matterª2013 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cortex.2013.10.007
In spite of their severely impaired episodic memory, patients with TGA benefit from the enactment effect. These results are discussed in relation to the role of motor components and episodic integration in memory for actions. We suggest that enactment effect can be used in clinical practice and rehabilitation, possible even for patients with a massive memory impairment.
ª2013 Elsevier Ltd. All rights reserved.
1. Introduction
Transient global amnesia (TGA) is a neurological syndrome that occurs in middle age and lasts up to 24 h. Its aetiology remains elusive, despite recent evidence of transient focal abnormalities in the CA1 hippocampal region (Bartsch et al, 2008). This amnesia is characterized by the sudden onset of massive anterograde amnesia with no attendant neurological or cognitive impairments (Quinette, Guillery-Girard, Dayan et al., 2006). During the acute phase, patients also display increased anxiety and a deterioration in mood, which have a deleterious impact on episodic memory functioning (Noe¨l et al., 2008).
Despite the massiveness of the episodic memory deficit, which is present whatever the types of materials that have to be memorized and whatever the encoding and retrieval con- ditions, TGA patients have been shown to be capable of acquiring new skills in procedural memory (Eustache et al., 1997), the perceptual representation system (Kazui &
Tanabe, 1995), and semantic memory (Beauregard, Weiner, Gold, & Chertkow, 1997; Guillery et al., 2001), using priming effects. No study, however, has ever investigated whether TGA patients can improve their episodic memory perfor- mance during the amnesic episode.
In the past three decades, many studies have focused on memory for actions (for a review, see Engelkamp, 1998;
Nilsson, 2000), a particular form of episodic memory (Tulving, 2002; Zimmer et al., 2001). Most of them focused on enactment effect, an improvement of recall and recognition scores for action phrases (e.g., “put on a glove”, “move the pen to the right”) when participants perform the actions (subject- performed task or SPT) during encoding compared with classic condition under which participants merely listen to or read the phrases (verbal task or VT).
Of the few studies that have explored this memory for actions in pathological conditions (for review, seeHainselin, Quinette, & Eustache, 2013), the majority have demonstrated the robustness of the enactment effect in children with autistic spectrum disorders, Parkinson’s disease and frontal lobe syndrome and Korsakoff’s syndrome while only a little benefit was observed in schizophrenia and sometimes in Alzheimer’s disease, and in rats (Thompson, 1959). However, a patient with developmental amnesia (Gardiner, Brandt, Vargha-Khadem, Baddeley, & Mishkin, 2006) showed no enactment benefit, suggesting other functions than episodic memory might contribute to this effect.
Although the enactment effect has frequently been studied since the 1980’s, there is still no consensus on how it enhances memory (for review, seeMadan & Singhal, 2012), including if it is supported by episodic memory. There are two main schools
of thought: according toEngelkamp (2001), participants first have to plan the action, involving motor and visual informa- tion. This multimodal theory is supported by the advantage of SPTs over experimenter-performed tasks (EPTs), when healthy participants simply observe somebody else perform- ing the action. The planning component does, however, seem to be essential, but needs to be more extensively studied, for example by letting participants choose which actions to perform with the different objects. According toKormi-Nouri and Nilsson (2001), enactment enhances episodic integration, binding the action verbs and object nouns together. This
“glue” theory has mostly been studied by comparing well- integrated (“put the money in the wallet”) and poorly inte- grated (”put the money in the napkin”) actions (Mangels &
Heinberg, 2006). Although this second hypothesis is a very important topic of discussion, binding itself had never been assessed with a specific task.
Thus, the main aim of our study was to assess whether the enactment effect is sufficiently robust for it to be observed during a massive amnesia episode such as TGA. Our second objective was to gain a better understanding of how enact- ment enhances memory by investigating the functions that sustain the enactment effect on patients. To this end, we chose to assess binding with a specific task to test the “glue”
theory. Inhibition and shifting (as patients have to perform different actions and shift from one to the other), short-term
Table 1eClinical and demographic characteristics of individuals with TGA and controls.
Acute TGA (n¼16)
Day-after TGA (n¼8)
Healthy controls (n¼18)
Sex: women/men 13/3 4/4 13/5
Age in years:
mean (SD)
60.56 (5.42) 68.3a,b(6.45) 61.00 (6.48)
Level of education in years:
mean (SD)
11.56 (2.99) 10.00 (3.51) 10.56 (2.20)
Duration of TGA in hours:
mean (SD)
4.96 (3.37) 3.81 (2.5) /
No. recurrent patients
2 (Second episode)
1 (Second episode)
/
A comparison of the three groups showed an effect of Group on age, F(2, 39)¼5.05,p<.05. Apost hocTukey test showed this was due to the presence of older patients in the day-after group compared with the acute and healthy control groups.
a Significant difference from healthy control group.
b Significant difference from acute TGA group.
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memory and episodic memory itself, thought to influence enactment effect, were also assessed. Given the impact of patients’ emotional state on memory, especially during TGA, we also wondered whether anxiety and mood might diminish the enactment effect.
2. Methods
2.1. ParticipantsTwenty-four TGA patients admitted to the emergency de- partments of Caen and Rouen University Hospitals between June 2010 and March 2012 were included in the study. Of these patients, 16 were in the acute phase (acute) and eight in the post-acute phase (day-after). Descriptive data are re- ported in Table 1. Eight of them (six acute and two day- after) were drawn from the cohort of a previously pub- lished study of awareness of memory failure (Hainselin et al., 2012). The control group consisted of 18 healthy in- dividuals. All participants gave their written informed consent to the study, which was approved by the local ethics committee.
All patients met the standard clinical criteria for the diag- nosis of TGA published byHodges and Warlow (1990). The 16 acute patients were examined during the TGA episode itself, and the eight day-after patients were assessed at the end of the episode. For all patients, a follow-up examination was carried out two months later (mean interval ¼ 69.59 days, SD¼9.13). By that stage, none of the patients exhibited any memory impairment. Finally, at the first test session, patients and controls underwent an assessment of two potentially confounding factors, namely visuoconstructive abilities (Signoret et al., 1989) and apraxia (Peigneux & Van der Linden, 2000). No impairment was found (data not shown). The acute patients were matched with healthy controls for sex, age and level of education.
2.2. Memory for action task
Participants incidentally encoded 48 object-action sentences (see Table 2 for an example of a complete list of items) under four conditions: VT, EPT, SPT and self-performed task with choice (SPTc; seeFig. 1for the general design and task details).
Immediate retrieval was assessed for each object-action sentence via cued recall (CR), recognition and source Table 2eExample of an entire list of 48 object-action
sentences used for the enactment effect task.
French English translation
De´placer le de´odorant derrie`re l’ordinateur
Move the deodorant behind the computer
De´placer l’allumette a` droite Move the match to the right Prendre le marteau entre le
pouce et l’index
Grab the hammer with the thumb and forefinger Serrer la boucle d’oreille dans la
main
Tighten the earring in the hand
Une action de votre choix avec l’e´lastique
An action you choose with the elastic
Frotter le taille-crayon Rub the pencil sharpener Une action de votre choix avec
le niveau
An action you choose with the spirit level
Caresser la balle de ping-pong Caress the ping-pong ball
Essuyer le bonbon Wipe the candy
Soupeser le thermome`tre Heft the thermometer Tordre le filtre a` cafe´ Twist the coffee filter Appuyer sur le couteau avec
l’index
Press the knife with the forefinger
Lancer le trombone en l’air Toss the paperclip Une action de votre choix avec
les ciseaux
An action you choose with the scissors
Tourner le me`tre dans le sens antihoraire
Turn the ruler counterclockwise Une action de votre choix avec
la cassette
An action you choose with the tape
Pincer la cle´ Pinch the key
Retourner la pince Upturn the pliers Une action de votre choix avec
l’e´ponge
An action you choose with the sponge
Ecraser la gomme avec la main Crush the eraser with the hand
Une action de votre choix avec la pile
An action you choose with the battery
Taper sur le bureau avec le crayon de couleur
Thump the desk with the coloured pencil
Plier la carte Bend the card
Passer la cuille`re d’une main a`
l’autre
Pass the spoon from one hand to the other
Souffler sur le tube de dentifrice Blow on the toothpaste tube Une action de votre choix avec
le gant
An action you choose with the glove
Une action de votre choix avec le bouton
An action you choose with the button
De´placer les lunettes a` gauche Move the glasses to the left Jeter la craie par terre Throw the chalk on the floor Mettre le bonnet dans la main Put the bonnet in the hand Une action de votre choix avec
la brosse a` dents
An action you choose with the toothbrush
Poser le peigne par terre Put the comb on the floor Poser le coton tige sur la chaise Put the swab on the chair Palper la lime a` ongles Palpate the nail file Donner le rasoir a` la personne
en face
Give the razor to the person in front of you
Ramener le savon vers soi Take the soap back to oneself
Tapoter le collier Tap the necklace
Visser avec la bague Screw with the ring Une action de votre choix avec
l’agrafeuse
An action you choose with the stapler
Secouer le cahier Shake the notebook
Gratter la louche Scratch the ladle
Cacher le tournevis Hide the screwdriver
Table 2e(continued)
French English translation
Pousser le te´le´phone Push the phone Une action de votre choix avec
la bougie
An action you choose with the candle
Faire rouler la fourchette Make the fork roll Tourner le pinceau dans le sens
horaire
Turn the paintbrush clockwise
Une action de votre choix avec le bracelet
An action you choose with the bracelet
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memory (free recall) tasks. We collected and analysed the CR and total recall (correct responses on CRþrecognition) scores.
For correctly recalled or recognized items, we collected and analysed R/K/G and source memory scores to assess the par- ticipants’ subjective experience.
2.3. Complementary cognitive assessment
The neuropsychological protocol was designed to assess binding, executive functions, short-term memory and episodic memory. Due to the specific nature of TGA, the cognitive assessment was modular and could be applied to the patients in the form of short sequences interleaved with medical examinations.
Binding, a process thought to take place in the episodic buffer, was assessed using a verbal and visuospatial
association task (for complete description, see Quinette, Guillery-Girard, Noe¨l et al., 2006; Quinette et al., 2013) (see Supplementary material).
Episodic memory was assessed with the Encoding e Storage e Retrieval (ESR) test, to which we added a Remember/Know/Guess (R/K/G; Gardiner, Ramponi, &
Richardson-Klavehn, 1998) paradigm (the R, K and G scores are expressed as percentages in the statistical analysis).
This has been used and described in previous studies of TGA (Hainselin et al., 2011; Quinette, Guillery-Girard, Noe¨l et al., 2006).
We investigated two executive functions, namely inhibi- tion and shifting, using the Stroop test and the Trail Making Test, respectively (Godefroy, 2008). Forward digit and forward visuospatial span tasks (Wechsler, 1991) were used to probe short-term memory.
Fig. 1eGeneral design of the memory for action task. Forty-eight action verbs and 48 objects were used in this task, paired in a semi-random way so as to avoid typical/well-integrated (“write with the pen”), dangerous (“throw the hammer in the air”) or impossible (“twist the cell phone”) utilisations of each item. We created 20 different lists of 48 object-action sentences, randomly attributed to each participant. Four extra object-action sentences (one for each condition described below) were used for training prior to the task to check that the participants understood the instructions. To ensure incidental encoding, participants were not aware they had to remember either actions or objects. During the encoding phase, an object was placed on a table in front of the participant and a sentence describing the relevant object-action pair was shown on a computer screen for 5 s, using E-Prime software. The design included four encoding conditions (mixed within each list). In the VT condition, participants read aloud the sentence displayed on the computer (no action performed), and in the EPT condition, they watched the experimenter performing the action displayed on the screen. In the
SPT condition, however, participants actually performed the action displayed on the computer, and in the SPTc condition, they both chose and performed an action with each item named on the computer screen. We expected the latter condition to enhance the effect, in line withEngelkamp’s (2001)theory on action planning. Immediately after the 48 trials, all the objects were brought out again and their names were displayed on the computer, one after the other (in a different random order from that of the encoding phase to avoid an order effect). In this CR phase, participants had to remember the action associated with each object. In the case of a wrong answer, the correct sentence was displayed on the screen, along with two nonstudied distractor sentences, and participants had to select the right one (recognition). Immediately after each correctly recalled or recognized item, we assessed the participants’ source memory by asking them to recall the encoding context of each sentence (read: VT; seen: EPT; self-performed: SPT; or self-performed with choice: SPTc). Their scores were expressed as a percentage of the maximum possible score. For each correctly recalled or recognized item (in CR or recognition), we also administered a Remember/Know/Guess (R/K/G) paradigm to assess the participants’ subjective experience of the retrieval process (the R, K and G scores for all tasks are expressed as percentages in the statistical analysis).
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2.4. Anxiety and mood assessments
State and trait anxiety was assessed by means of the State- Trait Anxiety Inventory (STAI:Spielberger, 1983). Mood state was evaluated by means of the Beck Depression Inventory (BDI; Beck, Rial, & Rickets, 1974) and the Befindlichkeits- Skala adjective mood scale (Bf-S Von Zerssen, Koeller, &
Rey, 1970).
Total duration for all tests administered was about 3 h.
2.5. Statistical methodology
The statistical analysis of the memory for action task scores was carried out using repeated-measures ANOVA, with Group (acute TGA, day-after TGA, healthy controls) as the between- participants factor and Condition (VT, EPT, SPT, SPTc) as the within-participants factor. The remaining data were analysed using a one-way ANOVA, with Group as a between- participants factor.Post hocTukey tests were used to carry out paired comparisons.
Pearson correlation coefficients were conducted on the acute TGA group to determine which processes were involved in the enactment effect. To this end, we calculated twoim- provements by actionindices (we deliberately chose not to use the expressionenactment effect to avoid confusion between these indices and the differences between the SPT and VT conditions in the memory for action task described above).
Theclassic action improvementindex (SPT/VT) was calculated by dividing the total score in the SPT condition by the total score in the VT condition. Thechosen action improvementindex (SPTc/
VT) was calculated by dividing the total score in the SPTc condition by the total score in the VT condition.
3. Results
3.1. Memory for action task
For the CR score, we found a main effect of Group, F(2, 39) ¼ 128.09, p < .0001, and Condition, F(3, 39) ¼ 36.40, p < .0001, but no Group Condition interaction, F(6, 117)¼1.79,p¼.11. Results are set out inTable 3.
Analyses of the total score (CRþrecognition) showed a main effect of Group,F(2, 39)¼30.72,p<.0001, and Condition, F(3, 39)¼20.67,p<.0001, but no GroupCondition interac- tion,F(6, 117)¼.85,p¼.54. Results are set out inTable 4.
In this condition, we observed the classic enactment effect (SPT>VT), as well as the chosen enactment effect (SPTc>VT), both for acute patients and for healthy controls.Post hocTukey tests also revealed better performances under the SPTc con- dition than under the EPT one by the acute patient group. No difference was found between the conditions within the day- after group.
The acute group performed more poorly than the healthy controls in all four conditions, and more poorly than the day- after group in the VT and SPT conditions.
Regarding the R/K/G paradigm, we found a main effect of Condition,F(2, 39)¼27.46,p<.0001, a trend towards a Group effect, F(2, 39) ¼ 2.96, p ¼ .065, and a Group Condition interaction, F(4, 68)¼ 8.80, p< .0001. Post hoc Tukey tests showed that patients in the acute phase of TGA gave more %G answers than %R or %K answers. We also found that acute patients gave fewer %K answers and more %G answers than the healthy controls did.
Concerning the source memory score, we found a signifi- cant main effect of Group, F(2, 39) ¼ 16.64, p< .0001, and Condition,F(3, 39)¼2.80,p<.05, but no GroupCondition interaction,F(6, 117)¼.98,p¼.45.Post hocanalyses revealed that healthy controls had better source memory perfor- mances in the SPT condition compared with the acute pa- tients, and better performances in the EPT condition compared with the day-after patients. Intragroup compari- sons did not reach statistical significance for any of the three groups (seeSupplementary material).
3.2. Complementary cognitive assessment
The detailed scores for cognitive and anxiety assessments are set out inTable 5.
As expected, a significant effect of Group was found in ESR for the immediate CR,F(2, 39)¼3.78,p<.05, free recall,F(2, 39)¼21.96,p<.0001, and recognition scoresF(2, 39)¼15.40, p<.0001 (Table 3), with poorer performances for acute pa- tients. The analysis of R/K/G paradigm performances revealed a significant effect of Group on the %R, F(2, 39) ¼ 21.19, p<.0001, and %G scores,F(2, 39)¼787,p¼.02, but not on the % K scores,F(2, 39)¼13.30,p¼.46, with lower %R and higher %G scores for acute patients than the other groups.
No statistical difference was found between the three groups in performances on the binding task, Stroop interfer- ence test, Part B of the TMT, forward digit span or forward visuospatial span.
Table 3eCR scores of patients and healthy controls in all memory for action conditions.
Acute TGA (n¼16) Day-after TGA (n¼8) Healthy controls (n¼18)
VT: number of correct responses (SD) .81a,b(0,46) 3.75a(.99) 7.69 (.85)
EPT: number of correct responses (SD) .69a,b(.35) 5.25a(1.58) 9.31 (.80)
SPT: number of correct responses (SD) 1.94a,b(1.06) 5.38a(1.28) 10.46c(.53)
SPTc: number of correct responses (SD) 4.06a,b,c,d,e(1.20) 7.38a,c(1.00) 11.23c,d(.55)
a Significant difference from healthy control group in the same condition.
bSignificant difference from day-after group in the same condition.
c Significant difference with VT condition within the same group (enactment effect).
dSignificant difference with EPT condition within the same group.
e Significant difference with SPT condition within the same group.
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3.3. Anxiety and mood assessments
Unlike trait-STAI, we found a significant difference between groups in scores on the state-STAI,F(2, 39)¼13.51,p<.0001, BDI, F(2, 39)¼3.36,p<.05, and Bf-S,F(2, 39)¼10.24,p<.001.Post hoc analyses showed that the acute patients scored more highly on the state-STAI, BDI and Bf-S than the healthy controls.
3.4. Correlations
For acute patients, regarding the SPT/VT action improvement index, negative correlations (p<.05) were found with incor- rect responses on the binding task (r¼ .73; i.e., the fewer incorrect responses provided by patients in the binding task, the more their memory was enhanced in the SPT condition) and state anxiety (r¼ .94; i.e., the less anxious patients were, the more their memory was enhanced in the SPT condition).
Moreover, a correlation was found between the SPTc/VT ac- tion improvement index and the forward visuospatial span score (r¼.90). No other significant correlations were found (seeTable 6).
4. Discussion
The results of the present study show that, despite their se- vere episodic memory impairment, TGA patients can still benefit from the enactment effect. This is the first time that this effect has been demonstrated in a sample of patients with such a pure and massive episodic memory deficit. We also highlighted links between the enactment effect and binding.
We discuss below the implications of these results at both theoretical and clinical levels.
The first aim of this study was to assess the enactment effect in TGA (i.e., better recall for actions that are actually performed rather for ones that are just verbally encoded).
The main finding was that TGA patients in the acute phase can benefit from SPT conditions just as much as healthy controls, even if they still do not perform normally. We labelled this enactment effect (SPT>VT)classic, to distin- guish it from thechosen enactment effect (SPTc>VT) dis- cussed below. Our results confirm that this classic enactment effect is present in amnesia, consistent with findings from Korsakoff patients (Mimura et al., 1998), allowing us to conclude that it is not impaired by amnesia per se. In our study, we went one step further, as this is the first time that the enactment effect has been found in a very
pure, nonpermanent amnesia without any cognitive reorganization.
In addition to the classic enactment effect (SPT>VT), we observed a chosen enactment effect (SPTc>VT) in the acute patients, even for CR. However, this chosen enactment effect may also have been due to the very high rate of typical actions, which are known to be well-integrated (Mangels & Heinberg, 2006) and more familiar. Future studies will need to address this issue by distinguishing between typical or well-integrated and poorly integrated actions, as well as the self-reference effect, in the new SPTc condition proposed here. We there- fore only discuss theclassicenactment effect below, from the perspective of their underlying cognitive functions.
Our second objective was to gain a better understanding of the cognitive functions that sustain memory enhancement in the enactment effect. First, we highlighted a link between a specific binding task and the classic enactment effect (assessed with the SPT/VT action improvement index). This result suggests the involvement of the episodic buffer in the enactment effect and is consistent with the episodic integra- tion view discussed below (Kormi-Nouri & Nilsson, 1998).
The classic enactment effect (SPT>VT) found in the acute patients and the healthy control group, added to the absence of any significant improvement between the VT and EPT conditions for any of the groups, is consistent with the hy- pothesis that the enactment effect has a motor component (Engelkamp, 2001), even in the absence of any improvement between the EPT and SPT conditions (Feyereisen, 2009).
Regarding glue theory, which assumes that enactment encoding cements actions and objects together (Kormi-Nouri
& Nilsson, 2001), the close correlation found between bind- ing scores and the SPT/VT action improvement index is consistent with the notion that binding plays a role in the enhancement of memory for actions in TGA patients. Thus, we suggest that both the motor control component and episodic integration processes (binding) contribute to the classic enactment effect seen in TGA patients. Our results support the idea of a spared episodic buffer (Quinette, Guillery-Girard, Noe¨l et al., 2006) for the classic enactment effect to occur.
By contrast, spared episodic memory may not be required for enactment effect. In the acute group, we did not observe any link between episodic memory scores and the action improvement indices or improvement in source memory be- tween VT and SPT. We suggest that, instead of stemming from a genuine episodic improvement, the enactment effect is sustained by implicit mechanisms, consistent with massive
Table 4eTotal scores (CRDrecognition scores, CRDR) of patients and healthy controls in all memory for action conditions.
Acute TGA (n¼16) Day-after TGA (n¼8) Healthy controls (n¼18)
VT: number of correct responses (SD) 4.25a,b(.85) 7.88 (.68) 8.46 (1.01)
EPT: number of correct responses (SD) 5.06a,b(1.09) 8.63 (.46) 9.77 (.55)
SPT: number of correct responses (SD) 6.75a,c(1.50) 9.38 (.96) 10.77c(.51)
SPTc: number of correct responses (SD) 7.81a,c,d(1.51) 9.75 (.88) 11.31c(.43)
a Significant difference from healthy control group in the same condition.
b Significant difference from day-after group in the same condition.
c Significant difference with VT condition within the same group (enactment effect).
d Significant difference with EPT condition within the same group.
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episodic memory impairment and implicit memory preser- vation in TGA (Eustache et al., 1997), or by semantic memory (Beauregard et al., 1997; Guillery et al., 2001). Nevertheless Jon, with spared semantic memory (Gardiner et al., 2006), did not benefit from enactment effect for action phrases (without object) recognition. Those results suggest that enactment ef- fect needs episodic buffer, but can occur independently of, or is only sparsely influenced by, episodic memory. The role of semantic memory and implicit mechanisms need to be explored in future researches.
Moreover, we found a negative correlation between the SPT/VT action improvement index and state-anxiety score.
This suggests an influence of state-anxiety on enactment ef- fect, with a more important effect for the less anxious pa- tients, although every patient showed better performances for SPT compared to VT. Besides supporting the importance of state-anxiety level on memory performances during TGA
(Hainselin et al., 2011; Noe¨l et al., 2008), it reinforces the robustness of enactment effect, which can be found even in anxious (and amnesic) patients.
In conclusion, the present experiment demonstrated that the enactment effect is robust enough to be found during a TGA episode. Our newly designed paradigm, featuring an original condition and a source memory assessment, in addition to a neuropsychological assessment, helped us to refine current understanding of the enactment effect. Further studies are now needed to 1) undertake a more in-depth exploration of enactment effect and its links with cognitive and emotional factors, and 2) integrate these very robust ef- fects into clinical practice and rehabilitation, possible even for patients with a massive memory impairment.
Study funding
This work was supported by Caen University Hospital, as part of a clinical research project. INSERM managed the PhD funding of Mathieu Hainselin, provided by Lower Normandy Regional Council and the Vicq d’Azyr association.
Conflict of interest
There is no competing interest.
Acknowledgements
The authors would like to thank Sandrine Bioux, Evangeline Bliaux, Carole Girard and Sophie Longeray for collecting the data.
We are also grateful to the staff of the Accident and Emergency Department, Neurology Units and Clinical Research Department at Caen University Hospital, and the Table 5eParticipants’ neuropsychological results expressed as means (SD).
Acute TGA (n¼16) Day-after TGA (n¼8) Healthy controls (n¼18)
Binding: incorrect answers 5.20 (4.84) 5.13 (4.02) 6.36 (3.41)
Stroop interference: time 133.06 (24.73) 135.00 (32.01) 122.85 (36.96)
Stroop interference: errors 2.50 (1.93) 2.38 (1.51) 3.31 (2.87)
TMT B: time 105.13 (27.14) 117.13 (59.08) 93.85 (34.30)
TMT B: errors .60 (.74) .75 (.89) .38 (.65)
Forward digit span 5.06 (1.24) 5.71 (1.11) 5.46 (.77)
Forward visuospatial span 5 (.63) 5.29 (2.92) 5.15 (.98)
ESR CR 12.94a(3.19) 14.63 (1.30) 15.85 (.38)
ESR free recall 3.19a,b(2.70) 6a(1.86) 8.85 (1.9)
ESR recognition 9.56a,b(4.77) 14.38 (1.30) 15.92 (.27)
ESR %R 25.38a,b(33.18) 64.66a(22.87) 71.36 (22.45)
ESR %K 34.03 (19.23) 23.58 (22.92) 23.44 (12.74)
ESR %G 40.59a,b(45,55) 11.76 (13.39) 6.20 (3.22)
Trait-STAI 43.5 (6.23) 39.63 (8.73) 37.54 (6.64)
State-STAI 49.75a(13.85) 41.50a(10.74) 28 (7.07)
BDI 5.69a(3.91) 4.38 (1.85) 2.46 (3.23)
Bf-S adjective mood scale 28.73a(10.09) 22.00 (7.40) 8.38 (7.39)
a Significant difference from healthy control group.
bSignificant difference from day-after group.
Table 6eCorrelations between action improvement index (SPT/VT), neuropsychological scores, anxiety and mood scales in patients during TGA (rvalues).
SPT/VT index SPTc/VT index
Binding: incorrect answers .73a .47
Stroop interference: time .10 .28
Stroop interference: errors .75 .20
TMT B: time .33 .51
TMT B: errors .33 .03
Forward digit span .25 .74
Forward visuospatial span .30 .90a
ESR CR .66 .01
ESR free recall .52 .53
ESR recognition .58 .26
Trait-STAI .30 .58
State-STAI .94a .77
BDI .08 .65
Bf-S adjective mood scale .24 .27
a Significant correlationp<.05.
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Emergency Neurology Unit at Rouen University Hospital for their unstinting cooperation.
Supplementary data
Supplementary data related to this article can be found at http://dx.doi.org/10.1016/j.cortex.2013.10.007.
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